Abstract
Polyandry in honeybee queens (Apis) causes many patrilines (subfamilies) within a colony, which may lead to a potential conflict of interest among workers. This may be most apparent during queen rearing when nepotistic worker behavior could influence the genetics of future generations. Several studies have searched for such conflict in European honeybees (A. mellifera), but studies on other Apis species remain lacking. We investigated the presence of reproductive conflict in A. cerana japonica by comparing the patriline proportion of queen larvae to that of adult workers. We determined the patrilines of 272 workers and 57 queen larvae using four polymorphic microsatellite markers that were sampled from queenless colonies originally derived from four naturally mated queen-right colonies. The number of patrilines in each colony was 9, 12, 8, and 7, respectively, which is lower than that observed in continental Asia. We found no difference in patriline proportion between adult workers and queen larvae. Our data support neither genetic variance for royalty or existence of worker nepotism in A. cerana japonica.
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Beekman M., Calis J.N.M. and Boot W.J. 2000. Parasitic honeybees get royal treatment. Nature 404: 723
Blanford E.J. 1923. Chinese bees as we find them. Bee World 5: 104–106
Boomsma J.J. and Ratnieks F.L.W. 1996. Paternity in eusocial Hymenoptera. Phil. Trans. R. Soc. Lond. B 351: 947–975
Breed M.D., Welch C.K. and Cruz R.C. 1994. Kin discrimination within honey bee (Apis mellifera) colonies: an analysis of the evidence. Behav. Proc. 33: 25–40
Châline N., Arnold G., Papin C. and Ratnieks F.L.W. 2003. Patriline differences in emergency queen rearing in the honey bee, Apis mellifera. Insect. Soc. 50: 234–236
Châline N., Martin S.J. and Ratnieks F.L.W. 2004. Absence of nepotism toward imprisoned young queens during swarming in the honey bee. Behav. Ecol. 16: 403–409
Cole B.J. and Wiernasz D.C. 1999. The selective advantage of low relatedness. Science 285: 891–893
Estoup A., Solignac M. and Cornuet J.-M. 1994. Precise assessment of the number of patrilines and of genetic relatedness in honeybee colonies. Proc. R. Soc. Lond. B 258: 1–7
Franck P., Koeniger N., Lahner G., Crewe R.M. and Solignac M. 2000. Evolution of extreme polyandry: an estimate of mating frequency in two African honeybee subspecies, Apis mellifera monticola and A.m. scutellata. Insect. Soc. 47: 364–370
Franck P., Solignac M., Vautrin D., Cornuet J.-M., Koeniger G. and Koeniger N. 2002. Sperm competition and last-male precedence in the honeybee. Anim. Behav. 64: 503–509
Goodisman M.A.D., Kovacs J.L. and Hoffman E.A. 2007. Lack of conflict during queen production in the social wasp Vespula maculifrons. Mol. Ecol. 16: 2589–2595
Goudet J. 2001. FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3)
Haberl M. and Tautz D. 1998. Sperm usage in honey bees. Behav. Ecol. Sociobiol. 42: 247–255
Harberl M. and Tautz D. 1999. Paternity and maternity frequencies in Apis mellifera sicula. Insect. Soc. 46: 137–145
Hughes W.O.H., Oldroyd B.P., Beekman M. and Ratnieks F.L.W. 2008. Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320: 1213–1216
Jordan L.A., Allsopp M.H., Oldroyd B.P., Wossler T.C. and Beekman M. 2008. Cheating honeybee workers produce royal offspring. Proc. R. Soc. B 275: 345–351
Keller L. and Reeve H.K. 1994. Genetic variability, queen number, and polyandry in social Hymenoptera. Evolution 48: 694–704
Koeniger N., Koeniger G. and Mardan M. 1994. Mimicking a honeybee queen? Vespa affinis indosinensis Perez 1910 hunts drones of Apis cerana F. 1793. Ethology 98: 149–153
Kraus F.B., Neumann P. and Moritz R.F.A. 2005. Genetic variance of mating frequency in the honeybee (Apis mellifera L.). Insect. Soc. 52: 1–5
Kraus F.B., Neumann P., van Praagh J. and Moritz R.F.A. 2004. Sperm limitation and the evolution of polyandry in the honeybee (Apis mellifera L.). Behav. Ecol. Sociobiol. 55: 494–501
Moritz R.F.A., Lattorff H.M.G., Neumann P., Kraus F.B., Radloff S.E. and Hepburn H.R. 2005. Rare royal families in honeybees, Apis mellifera. Naturwissenschaften 92: 488–491
Oldroyd B.P., Clifton M.J., Parker K., Wongsiri S., Rinderer T.E. and Crozier R.H. 1998. Evolution of mating behavior in the genus Apis and an estimate of mating frequency in Apis cerana (Hymenoptera: Apidae). Ann. Entomol. Soc. Am. 91: 700–709
Oldroyd B.P., Clifton M.J., Wongsiri S., Rinderer T.E., Sylvester H.A. and Crozier R.H. 1997. Polyandry in the genus Apis, particularly Apis andreniformis. Behav. Ecol. Sociobiol. 40: 17–26
Oldroyd B.P., Halling L.A., Good G., Wattanachaiyingcharoen W., Barron A.B., Nanork P., Wongsiri S. and Ratnieks F.L.W. 2001. Worker policing and worker reproduction in Apis cerana. Behav. Ecol. Sociobiol. 50: 3711–3377
Oldroyd B.P. and Wongsiri S. 2006. Asian Honey Bees. Harvard University Press, Cambridge, Mass. 340 pp
Osborne K.E. and Oldroyd B.P. 1999. Possible causes of reproductive dominance during emergency queen rearing by honeybees. Anim. Behav. 58: 267–272
Pamilo P. 1993. Polyandry and allele frequency differences between the sexes in the ant Formica aquilonia. Heredity 70: 472–480
Ratnieks F.L.W. and Reeve H.K. 1991. The evolution of queen-rearing nepotism in social Hymenoptera: effects of discrimination costs in swarming species. J. Evol. Biol. 4: 93–115
Sasaki K., Satoh T. and Obara Y. 1995. Sperm utilization by honey bee queens: DNA fingerprinting analysis. Appl. Entomol. Zool. 30: 335–341
Sasaki M. 1999. Wonders of the Japanese Honeybee—Biology of Northernmost Apis cerana. Kaiyusha Publishers, Tokyo. 191 pp (in Japanese)
Schneider S.S. and DeGrandi-Hoffman G. 2003. The influence of paternity on virgin queen success in hybrid colonies of European and African honeybees. Anim. Behav. 65: 883–892
Smith C.R., Toth A.L., Suarez A.V. and Robinson G.E. 2008. Genetic and genomic analyses of the division of labour in insect societies. Nat. Rev. Genet. 9: 735–748
Strassmann J.E. 2001. The rarity of multiple mating by females in the social Hymenoptera. Insect. Soc. 48: 1–13
Takahashi J., Shimizu S., Koyama S., Kimura K., Shimizu I. and Yoshida T. 2009. Variable microsatellite loci isolated from the Asian honeybee, Apis cerana (Hymenoptera; Apidae). Mol. Ecol. Res. doi:10.1111/j.1755-0998.2009.02268.x
Tarpy D.R., Gilley D.C. and Seeley T.D. 2004. Levels of selection in a social insect: a review of conflict and cooperation during honey bee (Apis mellifera) queen replacement. Behav. Ecol. Sociobiol. 55: 513–523
Tilly C.A. and Oldroyd B.P. 1997. Unequal subfamily porportions among honey bee queen and worker brood. Anim. Behav. 54: 1483–1490
Walsh P.S., Metzger D.A. and Higuchi R. 1991. Chelex (R)100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10: 507
Wang J. 2004. Sibship reconstruction from genetic data with typing errors. Genetics 166: 1963–1979
Wenseleers T. 2007. Nepotism absent in insect societies—or is it? Mol. Ecol. 16: 3063–3065
Yoshida T. 2005. Investigating the Society of Japanese Honeybees. Tamagawa Univ. Press. Tokyo. 141 pp (in Japanese)
Zar J.H. 1999. Biostatistical Analysis. Prentice Hall, Upper Saddle River, New Jersey, 663 pp
Acknowledgment
We thank B. Oldroyd, R. Gill and R. Hammond for their comments on the manuscript. We also thank T. Satoh and N. Kanda for their continuous help for SK.
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Koyama, S., Takagi, T., Martin, S.J. et al. Absence of reproductive conflict during queen rearing in Apis cerana . Insect. Soc. 56, 171–175 (2009). https://doi.org/10.1007/s00040-009-0008-2
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DOI: https://doi.org/10.1007/s00040-009-0008-2